Maturation of the human papillomavirus 16 capsid

mBio

Volumn 5, Issue 4, 2014, Pages 1-11

  Cardone, Giovanni ^a   Moyer, Adam L ^b   Cheng, Naiqian ^a   Thompson, Cynthia D ^b   Dvoretzky, Israel ^c   Lowy, Douglas R ^b   Schiller, John T ^b   Steven, Alasdair C ^a   Buck, Christopher B ^b   Trus, Benes L ^d  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c YALE UNIVERSITY   (United States)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; CAPSID PROTEIN;

ARTICLE; CAPSOMER; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CROSS LINKING; CRYOELECTRON MICROSCOPY; CYTOLYSIS; DISULFIDE BOND; HUMAN PAPILLOMAVIRUS TYPE 16; IMAGE ANALYSIS; IN VITRO STUDY; MAMMAL CELL; MOLECULAR DYNAMICS; NONHUMAN; VIRION; VIROGENESIS; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS MUTANT; CELL LINE; GROWTH, DEVELOPMENT AND AGING; HUMAN; PROTEIN SECONDARY STRUCTURE; ULTRASTRUCTURE;

HUMAN PAPILLOMAVIRUS - 16; HUMAN PAPILLOMAVIRUS TYPE 16; MIRIDAE;

CAPSID PROTEINS; CELL LINE; CRYOELECTRON MICROSCOPY; HUMAN PAPILLOMAVIRUS 16; HUMANS; PROTEIN STRUCTURE, SECONDARY; VIRION;

EID: 84908270074     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01104-14     Document Type: Article

References (43)

1. Jabłońska S, Majewski S, Obalek S, Orth G. 1997. Cutaneous warts. Clin. Dermatol. 15:309-319. http://dx.doi.org/10.1016/S0738-081X(96)00170-8.
2. Schiffman M, Kjaer SK. 2003. Chapter 2: natural history of anogenital human papillomavirus infection and neoplasia. J. Natl. Cancer Inst. Monogr. 31:14-19.
3. Arbyn M, de Sanjosé S, Saraiya M, Sideri M, Palefsky J, Lacey C, Gillison M, Bruni L, Ronco G, Wentzensen N, Brotherton J, Qiao YL, Denny L, Bornstein J, Abramowitz L, Giuliano A, Tommasino M, Monsonego J. 2012. EUROGIN 2011 roadmap on prevention and treatment of HPV-related disease. Int. J. Cancer 131:1969-1982. http://dx.doi.org/10.1002/ijc.27650.
4. Doorbar J. 2005. The papillomavirus life cycle. J. Clin. Virol. 32(Suppl 1):S7-S15. http://dx.doi.org/10.1016/j.jcv.2004.04.002.
5. Holmgren SC, Patterson NA, Ozbun MA, Lambert PF. 2005. The minor capsid protein L2 contributes to two steps in the human papillomavirus type 31 life cycle. J. Virol. 79:3938-3948. http://dx.doi.org/10.1128/JVI.79.7.3938-3948.2005.
6. Buck CB, Thompson CD, Pang YY, Lowy DR, Schiller JT. 2005. Maturation of papillomavirus capsids. J. Virol. 79:2839-2846. http://dx.doi.org/10.1128/JVI.79.5.2839-2846.2005.
7. Sapp M, Volpers C, Müller M, Streeck RE. 1995. Organization of the major and minor capsid proteins in human papillomavirus type 33 viruslike particles. J. Gen. Virol. 76:2407-2412. http://dx.doi.org/10.1099/0022-1317-76-9-2407.
8. Li M, Beard P, Estes PA, Lyon MK, Garcea RL. 1998. Intercapsomeric disulfide bonds in papillomavirus assembly and disassembly. J. Virol. 72: 2160-2167.
9. Sapp M, Fligge C, Petzak I, Harris JR, Streeck RE. 1998. Papillomavirus assembly requires trimerization of the major capsid protein by disulfides between two highly conserved cysteines. J. Virol. 72:6186-6189.
10. Steven AC, Heymann JB, Cheng N, Trus BL, Conway JF. 2005. Virus maturation: dynamics and mechanism of a stabilizing structural transition that leads to infectivity. Curr. Opin. Struct. Biol. 15:227-236. http://dx.doi.org/10.1016/j.sbi.2005.03.008.
11. Belnap DM, Olson NH, Cladel NM, Newcomb WW, Brown JC, Kreider JW, Christensen ND, Baker TS. 1996. Conserved features in papillomavirus and polyomavirus capsids. J. Mol. Biol. 259:249-263. http://dx.doi.org/10.1006/jmbi.1996.0317.
12. Buck CB, Cheng N, Thompson CD, Lowy DR, Steven AC, Schiller JT, Trus BL. 2008. Arrangement of L2 within the papillomavirus capsid. J. Virol. 82:5190-5197. http://dx.doi.org/10.1128/JVI.02726-07.
13. Hagel L. 2001. Gel-filtration chromatography. Curr. Protoc. Protein Sci. Chapter 8:Unit 83. http://dx.doi.org/10.1002/0471140864.ps0803s14.
14. Buck CB, Pastrana DV, Lowy DR, Schiller JT. 2005. Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol. Med. 119:445-462. http://dx.doi.org/10.1385/1-59259-982-6:445.
15. Zhao Q, Wu S, Manger W, Gadam S. August 2002. Process for making human papillomavirus virus-like particles with improved properties. U.S. patent 6,436,402.
16. Shi L, Sanyal G, Ni A, Luo Z, Doshna S, Wang B, Graham TL, Wang N, Volkin DB. 2005. Stabilization of human papillomavirus virus-like par-ticles by non-ionic surfactants. J. Pharm. Sci. 94:1538-1551. http://dx.doi.org/10.1002/jps.20377.
17. Buck CB, Pastrana DV, Lowy DR, Schiller JT. 2004. Efficient intracellular assembly of papillomaviral vectors. J. Virol. 78:751-757. http://dx.doi.org/10.1128/JVI.78.2.751-757.2004.
18. Wolf M, Garcea RL, Grigorieff N, Harrison SC. 2010. Subunit interactions in bovine papillomavirus. Proc. Natl. Acad. Sci. USA 107: 6298-6303. http://dx.doi.org/10.1073/pnas.0914604107.
19. Modis Y, Trus BL, Harrison SC. 2002. Atomic model of the papillomavirus capsid. EMBO J. 21:4754-4762. http://dx.doi.org/10.1093/emboj/cdf494.
20. Buck CB, Trus BL. 2012. The papillomavirus virion: a machine built to hide molecular Achilles’ heels, p 403-422. In Rossmann MG, Rao VB (ed), Viral molecular machines, vol. XIV. Springer Verlag, Berlin, Germany.
21. Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC. 2000. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell 5:557-567. http://dx.doi.org/10.1016/S1097-2765(00)80449-9.
22. Hagensee ME, Yaegashi N, Galloway DA. 1993. Self-assembly of human papillomavirus type 1 capsids by expression of the L1 protein alone or by coexpression of the L1 and L2 capsid proteins. J. Virol. 67:315-322.
23. Trus BL, Roden RB, Greenstone HL, Vrhel M, Schiller JT, Booy FP. 1997. Novel structural features of bovine papillomavirus capsid revealed by a three-dimensional reconstruction to 9-A resolution. Nat. Struct. Biol. 4:413-420. http://dx.doi.org/10.1038/nsb0597-413.
24. Roden RB, Armstrong A, Haderer P, Christensen ND, Hubbert NL, Lowy DR, Schiller JT, Kirnbauer R. 1997. Characterization of a human papillomavirus type 16 variant-dependent neutralizing epitope. J. Virol. 71:6247-6252.
25. Carter JJ, Wipf GC, Benki SF, Christensen ND, Galloway DA. 2003. Identification of a human papillomavirus type 16-specific epitope on the C-terminal arm of the major capsid protein L1. J. Virol. 77:11625-11632. http://dx.doi.org/10.1128/JVI.77.21.11625-11632.2003.
26. Day PM, Thompson CD, Buck CB, Pang YY, Lowy DR, Schiller JT. 2007. Neutralization of human papillomavirus with monoclonal antibodies reveals different mechanisms of inhibition. J. Virol. 81:8784-8792. http://dx.doi.org/10.1128/JVI.00552-07.
27. Day PM, Gambhira R, Roden RB, Lowy DR, Schiller JT. 2008. Mechanisms of human papillomavirus type 16 neutralization by L2 crossneutralizing and L1 type-specific antibodies. J. Virol. 82:4638-4646. http://dx.doi.org/10.1128/JVI.00143-08.
28. Schiller JT, Day PM, Kines RC. 2010. Current understanding of the mechanism of HPV infection. Gynecol. Oncol. 118:S12-S17. http://dx.doi.org/10.1016/j.ygyno.2010.04.004.
29. Chen XS, Casini G, Harrison SC, Garcea RL. 2001. Papillomavirus capsid protein expression in Escherichia coli: purification and assembly of HPV11 and HPV16 L1. J. Mol. Biol. 307:173-182. http://dx.doi.org/10.1006/jmbi.2000.4464.
30. Heymann JB, Cheng N, Newcomb WW, Trus BL, Brown JC, Steven AC. 2003. Dynamics of herpes simplex virus capsid maturation visualized by time-lapse cryo-electron microscopy. Nat. Struct. Biol. 10:334-341. http://dx.doi.org/10.1038/nsb922.
31. Conway JF, Wikoff WR, Cheng N, Duda RL, Hendrix RW, Johnson JE, Steven AC. 2001. Virus maturation involving large subunit rotations and local refolding. Science 292:744-748. http://dx.doi.org/10.1126/science.1058069.
32. Duda RL. 1998. Protein chain mail: catenated protein in viral capsids. Cell 94:55-60. http://dx.doi.org/10.1016/S0092-8674(00)81221-0.
33. Ross PD, Cheng N, Conway JF, Firek BA, Hendrix RW, Duda RL, Steven AC. 2005. Crosslinking renders bacteriophage HK97 capsid maturation irreversible and effects an essential stabilization. EMBO J. 24: 1352-1363. http://dx.doi.org/10.1038/sj.emboj.7600613.
34. Buck CB, Thompson CD. 2007. Production of papillomavirus-based gene transfer vectors. Curr. Protoc. Cell Biol. Chapter 26:Unit 26.21. http://dx.doi.org/10.1002/0471143030.cb2601s37.
35. Galvani M, Hamdan M, Herbert B, Righetti PG. 2001. Alkylation kinetics of proteins in preparation for two-dimensional maps: a matrix assisted laser desorption/ionization-mass spectrometry investigation. Electrophoresis 22:2058-2065. http://dx.doi.org/10.1002/1522-2683(200106)22:10_2058::AID-ELPS2058_3.0.CO;2-Z.
36. Conway JF, Trus BL, Booy FP, Newcomb WW, Brown JC, Steven AC. 1993. The effects of radiation damage on the structure of frozen hydrated HSV-1 capsids. J. Struct. Biol. 111:222-233. http://dx.doi.org/10.1006/jsbi.1993.1052.
37. Baker TS, Cheng RH. 1996. A model-based approach for determining orientations of biological macromolecules imaged by cryoelectron microscopy. J. Struct. Biol. 116:120-130. http://dx.doi.org/10.1006/jsbi.1996.0020.
38. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612. http://dx.doi.org/10.1002/jcc.20084.
39. Schrodinger LLC. 2010. The PyMOL molecular graphics system, version 1.3r1. Schrodinger LLC, Portland, OR.
40. Humphrey W, Dalke A, Schulten K. 1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:33-38. http://dx.doi.org/10.1016/0263-7855(96)0018-5.
41. Trabuco LG, Villa E, Mitra K, Frank J, Schulten K. 2008. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16:673-683. http://dx.doi.org/10.1016/j.str.2008.03.005.
42. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kalé L, Schulten K. 2005. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26:1781-1802. http://dx.doi.org/10.1002/jcc.20289.
43. Heymann JB, Cardone G, Winkler DC, Steven AC. 2008. Computational resources for cryo-electron tomography in Bsoft. J. Struct. Biol. 161:232-242. http://dx.doi.org/10.1016/j.jsb.2007.08.002.